Songbirds learn precisely sequenced motor skills (songs) subserved by distinct brain areas, including the premotor cortical analog HVC, which is essential for producing learned song, and a 'cortical'-basal ganglia loop required for song plasticity. Inputs from these nuclei converge in RA (robust nucleus of the arcopallium), making it a likely locus for song learning. However, activity-dependent synaptic plasticity has never been described in either input. Using a slice preparation, we found that stimulation patterns based on singing-related activity were able to drive opposing changes in the strength of RA's inputs: when one input was potentiated, the other was depressed, with the direction and magnitude of changes depending on the relative timing of stimulation of the inputs. Moreover, pharmacological manipulations that blocked synaptic plasticity in vitro also prevented reinforcement-driven changes to song in vivo. Together, these findings highlight the importance of precise timing in the basal ganglia-motor cortical interactions subserving adaptive motor skills.